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Young, Intact and Nested Retrotransposons Are Abundant in the Onion and Asparagus Genomes

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Young, Intact and Nested Retrotransposons Are Abundant in the Onion and Asparagus Genomes View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by The University of North Carolina at Greensboro Archived version from NCDOCKS Institutional Repository http://libres.uncg.edu/ir/asu/ Young, Intact And Nested Retrotransposons Are Abundant In The Onion And Asparagus Genomes Authors: C. Vitte1, M. C. Estep, J. Leebens-Mack and J. L. Bennetzen Abstract Background and Aims Although monocotyledonous plants comprise one of the two major groups of angiosperms and include .65 000 species, comprehensive genome analysis has been focused mainly on the Poaceae (grass) family. Due to this bias, most of the conclusions that have been drawn for monocot genome evolution are based on grasses. It is not known whether these conclusions apply to many other monocots. Methods To extend our understanding of genome evolution in the monocots, Asparagales genomic sequence data were acquired and the structural properties of asparagus and onion genomes were analysed. Specifically, several available onion and asparagus bacterial artificial chromosomes (BACs) with contig sizes .35 kb were annotated and analysed, with a particular focus on the characterization of long terminal repeat (LTR) retrotransposons. Key Results The results reveal that LTR retrotransposons are the major components of the onion and garden aspara-gus genomes. These elements are mostly intact (i.e. with two LTRs), have mainly inserted within the past 6 million years and are piled up into nested structures. Analysis of shotgun genomic sequence data and the observation of two copies for some transposable elements (TEs) in annotated BACs indicates that some families have become particu-larly abundant, as high as 4–5 % (asparagus) or 3–4 % (onion) of the genome for the most abundant families, as also seen in large grass genomes such as wheat and maize. Conclusions Although previous annotations of contiguous genomic sequences have suggested that LTR retrotran- sposons were highly fragmented in these two Asparagales genomes, the results presented here show that this was largely due to the methodology used. In contrast, this current work indicates an ensemble of genomic features similar to those observed in the Poaceae. C. Vitte1, M. C. Estep, J. Leebens-Mack and J. L. Bennetzen (2013) "Young, Intact And Nested Retrotransposons Are Abundant In The Onion And Asparagus Genomes" Annals of Botany Version of Record Available At www.academic.oup.com [doi:10.1093/aob/mct155] INTRODUCTION extensively studied at the cytological and biochemical levels. Monocotyledonous plants are divided into 11 orders: Acorales, Onion is a diploid (2n 2x 16), but has a genome size of Alismatales, Petrosaviales, Dioscoreales, Pandanales, Liliales, approx. 16 400 Mb/1C, one of the largest among all cultivated Asparagales, Arecales, Poales, Commelinales and Zingiberales, the diploid species and similar in size to that of hexaploid wheat last four being grouped into the Commelinid clade (Stevens (http://data.kew.org/cvalues/). Although a large genome can fa- et al., 2001). Most of these orders include multiple agriculturally cilitate cytogenetic analyses, it has hampered the development of and ornamentally important groups. Among these, the Asparagales genomic resources, thus impeding both molecular breeding and may be the second most important for agriculture and horticulture characterization of the molecular origins of its large genome. after the Poales. The Asparagales includes the hyperdiverse Transcriptome analyses suggest that onion transcript characteris- Orchidaceae with .30 000 species and nearly 5000 additional tics are quite distinct from those of Poaceae (Kuhl et al., 2004), species distributed across the rest of the order. These include im- but little is known about the transposable element (TE) compos- portant crops such as aloe (Aloe vera), agave (Agave tequilana), ition in the onion genome. In particular, while long terminal asparagus (Asparagus officinalis), garlic (Allium sativum), repeat (LTR) retrotransposons are thought to be a major compo- leek (Allium ampeloprasum), onion (Allium cepa) and vanilla nent of the onion genome (Pearce et al., 1996), the role that TE (Vanilla planifolia), as well as ornamental plants such as yuccas, activity has played in shaping the current genome is poorly amarylids, daffodils, irises and orchids. With a world production understood. Most of the available data on onion genome compos- of .95 Mt, it is the third most cultivated group for vegetable pro- ition come from re-association kinetics (Cot) and fluorescence in duction in the world after the Solanales (including potato, situ hybridization (FISH) analyses that revealed an abundance of tomato, pepper and aubergine) and the Cucurbitales (including middle-repetitive sequences interspersed with low copy number melons, cucumbers and gourds) (world production, http:// regions (Stack and Comings, 1979; Pearce et al., 1996; Suzuki faostat.fao.org/). et al., 2001). Analyses of bacterial artificial chromosome Onion (A. cepa) is the most economically important member (BAC)-end sequences revealed a high frequency of TEs, consist- of the Asparagales. As a biological model, onion has been ent with results obtained for other plants with large genomes (Jaksˇe et al., 2008). Sequencing of a few onion BACs (Do et al., MATERIALS AND METHODS 2003; Jaksˇe et al., 2008) revealed the presence of repeated sequences, including a large quantity (approx. 50 %) of TEs, Sequence data but also microsatellites and direct tandem repeats. Most of the Contiguous sequences (contigs) from four asparagus (Asparagus TEs found were interpreted as highly degraded, a feature that is officinalis) BACs (available as GenBank accessions AC183410, quite different from the pattern observed in grasses, where DQ273271 and the overlapping AC183409 and AC183411) that intact and young (,5 million year old) elements are found. represent three genomic regions selected to contain a sulfite reduc- However, the scarcity of genomic data and the absence of any tase gene, a sucrose transporter gene and the AOB272 cDNA TE database from a closely related species made the detection (described in Jaksˇe et al., 2006), and three full-length onion of TEs in Asparagales particularly challenging. (Allium cepa) BACs (AB111058, DQ273272 and DQ273270) Garden asparagus (A. officinalis) is the third most economically were retrieved from NCBI. In addition, 3235 unpaired Sanger important plant in the Asparagales, after onion and garlic. It is shotgun sequences from onion were provided by C. Town, and believed to be native to Europe, northern Africa and Asia, and we generated an additional 3560 unpaired Sanger sequences is even more widely cultivated as a vegetable crop. Asparagus is from garden asparagus (deposited in GenBank). diploid (2n 2x 20) and has one of the smallest genomes of the core Asparagales (approx. 1300 Mb/1C, http://data.kew.org/ cvalues/) For this reason, garden asparagus has been proposed as Annotation of asparagus and onion BAC sequences a genomic model for the core Asparagales that would help inves- Bacterial artificial chromosome sequences were used as tigate the gene content of other Asparagales with larger genome the subject for Repeatmasker and BLASTX searches. The sizes, such as onion (Kuhl et al., 2005; Telgmann-Rauber et al., Repeatmasker search was performed with version 3.0 (Smit 2007). Synteny between asparagus and onion genomes has et al., 1996; http://www.repeatmasker.org) using repbase received preliminary investigation by mapping several onion (April 2012) and redat (MIPS, May 2008) as query databases. expressed sequence tags (ESTs) on both onion chromosomes For the BLASTX search (Altschul et al., 1990), version blastall and a few studied asparagus BACs (Jaksˇe et al., 2006). This ana- 2.2.25 was used with the nr database (March 2012) as query and a lysis posited that many genes encoding physically linked ESTs threshold e-value ≤1025, and without filtering out low complex- in asparagus were located on distinct chromosomes in onion, sug- ity regions. In parallel, asparagus and onion shotgun reads were gesting a lack of collinearity between the two genomes. Since the mapped onto the asparagus and onion BACs, respectively, in ESTs analysed were not single copy [e.g. from gene duplication, order to spot repeated regions that may have been missed by perhaps via TE mobilization of genes or gene fragments (Jin the BLASTX and Repeatmasker searches due to the absence of and Bennetzen, 1994; Jiang et al., 2004; Lai et al., 2005; Yang closely related TEs in the available repeat databases. For this, and Bennetzen, 2009)], it is possible that the sequences compared BLASTN searches using BAC sequences as subjects and were not orthologous. However, given that the divergence of the shotgun sequences as queries were performed. lineages leading to these species occurred approx. 87 million Foreach contig, results of these searches were visualized using years ago (Mya) (Jansson and Bremer, 2005), frequent inter- Argo v10.0.31 (http://www.broadinstitute.org/annotation/argo) ruptions in microcollinearity are expected (Bennetzen, 2000). and manually evaluated to provide a first annotation. Genes Hence, more detailed analyses, as well as comparison of other were predicted using the BLASTX results. Only matches to a species within the Asparagales, are needed to investigate and predicted protein from a dicotyledonous species with an e-value extend these results. ≤1025 were used, because, as onion and asparagus are mono- The recent sequencing
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